Survival and functionality of human induced pluripotent stem cell-derived oligodendrocytes in a nonhuman primate model for multiple sclerosis

Stem Cells Translational Medicine

Volumn 5, Issue 11, 2016, Pages 1550-1561

  Thiruvalluvan, Arun ^a   Czepiel, Marcin ^a   Kap, Yolanda A ^b   Mantingh Otter, Ietje ^a   Vainchtein, Ilia ^a   Kuipers, Jeroen ^a   Bijlard, Marjolein ^a   Baron, Wia ^a   Giepmans, Ben ^a   Brück, Wolfgang ^c   ’T Hart, Bert A ^a,b   Boddeke, Erik ^a   Copray, Sjef ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Multiple sclerosis; Myelination; Nonhuman primates; Oligodendrocytes

Indexed keywords

ALKALINE PHOSPHATASE; FIBROBLAST GROWTH FACTOR 2; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEOLIPID PROTEIN; TRANSCRIPTION FACTOR NKX2.2;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALLITRICHINAE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; MOUSE; MULTIPLE SCLEROSIS; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; STEREOTACTIC TREATMENT;

EID: 84992093413     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2016-0024     Document Type: Article

References (38)

1. Hauser SL, Chan JR, Oksenberg JR. Multiple sclerosis: Prospects and promise. Ann Neurol 2013;74:317-327.
2. Hemmer B, Archelos JJ, Hartung HP. New concepts in the immunopathogenesis of multiple sclerosis. Nat Rev Neurosci 2002;3:291-301.
3. Stys PK, Zamponi GW, van Minnen J et al. Will the real multiple sclerosis please stand up? Nat Rev Neurosci 2012;13:507-514.
4. Goldman SA, Nedergaard M, Windrem MS. Glial progenitor cell-based treatment and modeling of neurological disease. Science 2012; 338:491-495.
5. Uchida N, Chen K, Dohse M et al. Human neural stem cells induce functional myelination in mice with severe dysmyelination. Sci Transl Med 2012;4:155ra136.
6. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
7. Ogawa S, Tokumoto Y, Miyake J et al. Induction of oligodendrocyte differentiation from adult human fibroblast-derived induced pluripotent stem cells. In Vitro Cell Dev Biol Anim 2011;47:464-469.
8. Pouya A, Satarian L, Kiani S et al. Human induced pluripotent stem cells differentiation into oligodendrocyteprogenitorsandtransplantation in a rat model of optic chiasm demyelination. PLoS One 2011;6:e27925.
9. Wang S, Bates J, Li X et al. Human iPSCderived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013; 12:252-264.
10. Douvaras P, Wang J, Zimmer M et al. Efficient generation of myelinating oligodendrocytes fromprimary progressivemultiple sclerosis patients by induced pluripotent stem cells. Stem Cell Rep 2014;3:250-259.
11. Najm FJ, Madhavan M, Zaremba A et al. Drug-based modulation of endogenous stem cells promotes functional remyelination in vivo. Nature 2015;522:216-220.
12. Piao J, Major T, Auyeung G et al. Human embryonic stem cell-derived oligodendrocyte progenitors remyelinate the brain and rescue behavioral deficits following radiation. Cell Stem Cell 2015;16:198-210.
13. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 2008;9:839-855.
14. Jagessar SA, Kap YS, Heijmans N et al. Induction of progressive demyelinating autoimmune encephalomyelitis in common marmoset monkeys using MOG34-56 peptide in incomplete Freund adjuvant. J Neuropathol Exp Neurol 2010;69:372-385.
15. ’t Hart BA, Hintzen RQ, Laman JD. Preclinical assessment of therapeutic antibodiesagainst human CD40 and human interleukin-12/23p40 in a nonhumanprimatemodel ofmultiple sclerosis. Neurodegener Dis 2008;5:38-52.
16. Palazzi X, Bordier N. The marmoset brain in stereotaxic coordinates. New York: Springer-Verlag, 2008.
17. Sommer CA, Stadtfeld M, Murphy GJ et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. STEM CELLS 2009;27:543-549.
18. Hu Z, Li T, Zhang X et al. Hepatocyte growth factor enhances the generation of high-purity oligodendrocytes from human embryonic stem cells. Differentiation 2009;78: 177-184.
19. Pluchino S, Gritti A, Blezer E et al. Human neural stem cells ameliorate autoimmune encephalomyelitis in non-human primates. Ann Neurol 2009;66:343-354.
20. Sher F, Amor S, Gerritsen W et al. Intraventricularly injected Olig2-NSCs attenuate established relapsing-remitting EAE in mice. Cell Transplant 2012;21:1883-1897.
21. Sabelström H, Stenudd M, Réu P et al. Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 2013;342:637-640.
22. Pluchino S, Cossetti C. How stem cells speak with host immune cells in inflammatory brain diseases. Glia 2013;61:1379-1401.
23. Numasawa-Kuroiwa Y, Okada Y, Shibata S et al. Involvement of ER stress in dysmyelination of Pelizaeus-Merzbacher Disease with PLP1 missense mutations shown by iPSC-derived oligodendrocytes. Stem Cell Rep 2014;2: 648-661.
24. Einstein O, Grigoriadis N, Mizrachi-Kol R et al. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp Neurol 2006;198:275-284.
25. Cossetti C, Alfaro-Cervello C, Donegà M et al. New perspectives of tissue remodelling with neural stem and progenitor cell-based therapies. Cell Tissue Res 2012;349:321-329.
26. Donega M, Giusto E, Cossetti C et al. Systemic injection of neural stem/progenitor cells in mice with chronic EAE. J Vis Exp 2014 [Epub ahead of print].
27. Cusimano M, Biziato D, Brambilla E et al. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain 2012; 135:447-460.
28. Mendonça LS, Nóbrega C, Hirai H et al. Transplantation of cerebellar neural stem cells improves motor coordination and neuropathology in Machado-Joseph disease mice. Brain 2015;138:320-335.
29. Drago D, Cossetti C, Iraci N et al. The stem cell secretome and its role in brain repair. Biochimie 2013;95:2271-2285.
30. Kim WK, Kim D, Cui J et al. Secretomeanalysis of human oligodendrocytes derived from neural stem cells. PLoS One 2014;9:e84292.
31. Pluchino S, Zanotti L, Rossi B et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005;436: 266-271.
32. Cao W, Yang Y, Wang Z et al. Leukemiainhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. Immunity 2011;35:273-284.
33. Laterza C, Merlini A, De Feo D et al.: iPSC-derived neural precursors exert a neuroprotective role in immune-mediated demyelination via the secretion of LIF. Nat Commun 2013;4:2597-2613.
34. Nakatsuji N, Nakajima F, Tokunaga K. HLA-haplotype banking and iPS cells. Nat Biotechnol 2008;26:739-740.
35. Zimmermann A, Preynat-Seauve O, Tiercy JM et al. Haplotype-based banking of human pluripotent stem cells for transplantation: potential and limitations. Stem Cells Dev 2012; 21:2364-2373.
36. Fossati V, Douvaras P. Generating induced pluripotent stem cells for multiple sclerosis therapy. Regen Med 2014;9:709-711.
37. Douvaras P, Fossati V. Generation and isolation of oligodendrocyte progenitor cells from human pluripotent stem cells. Nat Protoc 2015;10:1143-1154.
38. Rao MS, Atala A. Developing induced pluripotent stem cell-based therapy for the masses. STEM CELLS TRANSLATIONAL MEDICINE 2016;5:129-131.